Infrared Heater System for Warming Tropical Forest Understory Plants and Soils

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Infrared heater system for warming tropical forest understory plants and soils

Bruce Kimball The Greenleaf Group

Auro M. Alonso-Rodriguez International Institute of Tropical Forestry

Molly A. Cavaleri Michigan Technological University, [email protected]

Sasha Reed Southwest Biological Science Center

Grizelle Gonzalez International Institute for Tropical Forestry

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Recommended Citation Kimball, B., Alonso-Rodriguez, A. M., Cavaleri, M. A., Reed, S., Gonzalez, G., & Wood, T. E. (2018). Infrared heater system for warming tropical forest understory plants and soils. Ecology and Evolution, 8(4), 1932-1944. http://dx.doi.org/10.1002/ece3.3780 Retrieved from: https://digitalcommons.mtu.edu/michigantech-p/461

Follow this and additional works at: https://digitalcommons.mtu.edu/michigantech-p Part of the Forest Sciences Commons Authors Bruce Kimball, Auro M. Alonso-Rodriguez, Molly A. Cavaleri, Sasha Reed, Grizelle Gonzalez, and Tana E. Wood

This article is available at Digital Commons @ Michigan Tech: https://digitalcommons.mtu.edu/michigantech-p/461

Received: 14 September 2017 | Revised: 28 November 2017 | Accepted: 8 December 2017 DOI: 10.1002/ece3.3780

ORIGINAL RESEARCH

Infrared heater system for warming tropical forest understory plants and soils

1The Greenleaf Group, Phoenix, AZ, USA Abstract 2International Institute of Tropical Forestry, USDA Forest Service, Luquillo, PR, The response of tropical forests to global warming is one of the largest uncertainties USA in predicting the future carbon balance of Earth. To determine the likely effects of el- 3School of Forest Resources and evated temperatures on tropical forest understory plants and soils, as well as other Environmental Science, Michigan Technological University, Houghton, MI, USA ecosystems, an infrared (IR) heater system was developed to provide in situ warming 4U.S. Geological Survey, Southwest Biological for the Tropical Responses to Altered Climate Experiment (TRACE) in the Luquillo Science Center, Moab, UT, USA Experimental Forest in Puerto Rico. Three replicate heated 4-m-diameter plots were 5International Institute for Tropical Forestry, USDA Forest Service, Río Piedras, warmed to maintain a 4°C increase in understory vegetation compared to three un- PR, USA heated control plots, as sensed by IR thermometers. The equipment was larger than

Correspondence any used previously and was subjected to challenges different from those of many Bruce A. Kimball, The Greenleaf Group, temperate ecosystem warming systems, including frequent power surges and outages, Phoenix, AZ, USA. Email [email protected] high humidity, heavy rains, hurricanes, saturated clayey soils, and steep slopes. The system was able to maintain the target 4.0°C increase in hourly average vegetation Funding information US Department of Energy, Grant/Award temperatures to within ± 0.1°C. The vegetation was heterogeneous and on a 21° Number: DE-SC-0011806 and DE- slope, which decreased uniformity of the warming treatment on the plots; yet, the SC0012000; USDA Forest Service, Grant/ Award Number: 11-DG-11120101-012, green leaves were fairly uniformly warmed, and there was little difference among 13-IA-11120101-008, 13-JV-11120101-033 0–10 cm depth soil temperatures at the plot centers, edges, and midway between. Soil and 14-JV-11120101-006; National Science Foundation, Grant/Award Number: DEB temperatures at the 40–50 cm depth increased about 3°C compared to the controls 1239764 and EAR-1331841 after a month of warming. As expected, the soil in the heated plots dried faster than that of the control plots, but the average soil moisture remained adequate for the plants. The TRACE heating system produced an adequately uniform warming precisely controlled down to at least 50-cm soil depth, thereby creating a treatment that allows for assessing mechanistic responses of tropical plants and soil to warming, with appli- cability to other ecosystems. No physical obstacles to scaling the approach to taller vegetation (i.e., trees) and larger plots were observed.

KEYWORDS climate change, global warming, heater array, infrared warming, proportional integrative derivative control, trees

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

.www.ecolevol.org Ecology and Evolution. 2018;8:1932–1944 | 1932 KIMBALL et al. | 1933

1 | INTRODUCTION experiments, soil incubations, and studies along elevation gradients (e.g., Chen, Yu, González, Zou, & Gao, 2017). While the use of field Ecosystems worldwide are responding to Earth’s changing climate, experimental warming has been less common in forested ecosystems, with important implications for their structure and function, as well it holds much promise for elucidating the consequences of increas- as for determining central feedbacks to future climate (IPCC, 2014). ing temperatures. The majority of forest warming experiments that These ongoing changes and associated consequences underscore the currently exist have primarily been implemented in temperate forests value of understanding and forecasting the effects of climatic change, using underground cables (Melillo et al., 2002; Pries, Castanha, Porras, yet our knowledge of how systems will respond to further increases & Torn, 2017) but there are other viable methods. Using infrared (IR) in temperature remains notably poor (e.g., Shao, Zeng, Sakaguchi, heaters is an approach to field warming that enables warming of the Monson, & Zeng, 2013). This is particularly true for tropical forested vegetation and soils under free-air, open-field conditions, with much ecosystems, which sustain exceptionally high biodiversity, cycle vast less disturbance than buried cables (e.g., Jarvi & Burton, 2013). IR amounts of carbon, and represent a key uncertainty in considering ter- arrays that maintain a constant temperature rise of the heated plots restrial ecosystem feedbacks to future climate (Cavaleri, Reed, Smith, above that of reference plots using proportional integrative derivative & Wood, 2015; Pan et al., 2011; Wood, Cavaleri, & Reed, 2012). (PID) control have been reported for several ecosystems including grass However, while the need for an improved understanding of warming (Nijs et al., 1996; Van Peer, Nijs, Reheul, & De Cauwer, 2004), tundra effects on tropical forests is clear, enhancing our understanding of (Marchand, Mertens, Kockelbergh, Beyens, & Nijs, 2005; Nijs et al., temperature effects on these and other ecosystems remains a signifi- 2000), grazing land (LeCain et al., 2015; Luo et al., 2010), wheat fields cant research challenge (Cavaleri et al., 2015). (Kimball et al., 2015; Wall, Kimball, White, & Ottman, 2011), paddy Common methods for investigating temperature controls over rice (Gaihre et al., 2014; Rehmani et al., 2011), soybean (Ruiz-Vera forest composition and processes include laboratory and greenhouse et al., 2013; Siebers et al., 2015), and maize (Ruiz-Vera, Siebers, Drag, Ort, & Bernacchi, 2015), as well as tree saplings (McDaniel et al., 2014; Rich et al., 2015). However, all of these studies had 3-m-diameter plots or smaller, and most warmed by only 1.5°C during daytime. Although short-term heat-wave simulations have achieved higher degrees of warming (e.g., De Boeck, Dreesen, Janssens, & Nijs, 2011; Marchand et al., 2005; Siebers et al., 2015; Van Peer et al., 2004), the highest reported season-long warming of a 3-m-diameter plot is 3.5°C (Ruiz- Vera et al., 2015). Our experimental system expanded plot size to 4 m diameter and the degrees of warming to 4°C. The projected warming in Puerto Rico is greater than the global averages (Henareh Khalyani et al., 2016). Further, we adapted an IR heater system for a wet tropical forest with high humidity, hurricanes, power surges and outages, clayey soils, and a steep slope. The solutions described herein address these challenges to warming tropical forest understory plants and soils and provide valuable information for designing future warming experiments for taller vegetation in a number of underrepresented ecosystem types.

2 | MATERIALS AND METHODS

2.1 | Site

The experimental site is located in northeastern Puerto Rico near the USDA Forest Service Sabana Field Research Station in the Luquillo Experimental Forest (LEF; 18°18′N, 65°50′W) (Figures 1 and 2). The site is classified as a subtropical wet forest according to the Holdridge Life Zone System (Holdridge, 1967) and is a secondary forest, regen- erated naturally from pasture since the early 1950s. Mean annual temperature is 24°C, with month-to-month variation of just 4°C, and FIGURE 1 Geographic site map showing location of Puerto Rico mean annual rainfall is 3,500 mm (García-Martino, Warner, Scatena, & with respect to continental United States and insert showing location of USDA Forest Service Sabana Field Research Station within Puerto Civco, 1996). While the driest period generally occurs from January to Rico March, there is no significant “dry season,” as every month receives 1934 | KIMBALL et al.

TABLE 1 Slopes of the soil surface in the various plots of the TRACE experiment (See Figure 2 for plot locations)

Plot Slope (°)

C1 20 H2 26 C3 15 H4 18 C5 16 H6 18 Weather Station 22

slippage down slope. The heaters were bolted to cross-bars (38 mm galvanized steel pipes), which spanned the space between posts on the periphery, and which enabled the heaters to face the center of the plots. The cross-bars were attached to the vertical posts with Kee Klamps (Kee Safety Inc., Buffalo, NY), allowing heaters to be mounted at the same height above the vegetation regardless of slope. The upslope and downslope heaters were deployed with long axes horizontal, while the long axes of the side heaters were parallel to the slope. The short axes of all heaters were tilted 45° with respect to their vertical support posts. The variability of the height of the vegetation provided another challenge, so heaters were mounted at 0.4 times plot diameter above three-fourth the height of the tallest plants to provide as uniform warming as possible without exposing the tallest vegetation to too much heat. A small junction box was installed for each heater and connected to a larger junction box for each heated plot via a waterproof, flexible “super service” cable. This cable along with the

FIGURE 2 Schematic plan to scale showing layout of plots in the use of Kee Klamps enabled the heaters to be raised and lowered for Luquillo Experimental Forest repairs and to adjust for changing vegetation heights. As specified by a civil engineer, the concrete footings, posts, and greater than 200 mm and precipitation is highly variable (Heartsill- cross-bars with the heaters should be able to withstand hurricane- Scalley, Scatena, Estrada, McDowell, & Lugo, 2007). Located at 100 m force winds with the heaters tilted vertical at a maximum operating elevation, the site is characterized by relatively steep slopes ranging height of 3.6 m with no allowance for a windbreak from the trees. from 15 to 26°, with an average slope of 21° (Table 1). Soils are classi- Nevertheless, when a hurricane is forecast, the plan is to shut off fied as Ultisols and are deep, clay-rich and acidic, with high aluminum the system and lower the heaters to just above vegetation height. and iron content (Scatena, 1989). Root biomass is concentrated During the time this study was undergoing journal review (September (>60%) in the top 10 cm of mineral soil (Silver & Vogt, 1993). 2017), Hurricanes Irma and Maria struck Puerto Rico, including the experimental site. Heaters were lowered in advance of the stronger Hurricane Maria but not for Irma. The structures withstood the winds 2.2 | Equipment of both hurricanes. However, falling trees and branches, for which The basic design of the IR heater system was that of the T-FACE there is no protection, damaged portions of the plot infrastructure, (temperature free-air controlled enhancement) described by Kimball the majority of which was to the supporting posts for the heaters. et al. (2008), which produced uniform warming across hexagonal plots Based on our observations from the two storms, the infrastructure with six IR heaters (Figure 3), and which was able to maintain a con- damage from fallen trees was more substantial when the heaters were stant temperature rise of the heated plots above that of control or not lowered. Nevertheless, all damage is repairable, and we expect the reference plots for growing-season-long periods of time. In our case, experiment will be operational again by the time power is restored to the slope (~21°; Table 1), saturated soils, and high clay content pro- the area. Thus, there is promise for the design even in areas where vided additional challenges. Galvanized 38 mm steel pipes (nominal disturbances such as hurricanes are common. 1½ inches) were installed to 0.7 m depth in 0.3 m × 0.8 m concrete Based on theory (Kimball, 2005) and experience (Kimball et al., 2008) footings for each of the six hexagon points. The footings and posts and the weather data available at the design stage, larger heaters were with attached cross-bars provided stable structures and prevented required to warm 4-m-diameter plots than had been used previously KIMBALL et al. | 1935

FIGURE 3 Photograph of a heated plot showing the understory vegetation beneath the tree canopy along with six infrared heaters deployed on pipes arranged in a hexagon. The vertical pipes are posts set in concrete footings, two of which are visible in the foreground. The gray control panel is to the right. In the background is the 480 V, 3-phase power line in yellow conduit. (Photo by Mónica Cruz) in such experiments. The selected heaters were rectangular black-body Anemometer radiators (Model Raymax 1010, Watlow Electric Manufacturing Co., St. Infrared thermometer Louis, MO [currently manufactured by Heat and Sensor Technology, Control panel H2 Lebanon, OH], 1,143 mm × 457 mm × 47.4 mm, 8,100 W, 480 V, 3- C1 1 1 phase). They were constructed of stainless steel and welded around the H4 edges to be liquid tight, with insulation behind the internal electrical C3 1 2 heating wires to minimize heat loss from the back. We requested that H6 the welded lip be around the hot front side because in our application C5 they are pointed downwards, and we wanted to minimize leaves and 1 3 other debris being caught by the lip. The emitting face was painted Mulplexor black, and the maximum watt density of 15.4 W/m2 ensures that they emit almost no radiation at wavelengths <850 nm, which may be photo- SDM-CV04 chromatically active in plants (Kimball, 2005; Kimball, Conley, & Lewin, CR1000 Interface makes Datalogger 2012). The three control or reference plots had identical posts and 0-10 V signals cross-bars to the three heated plots, but with dummy heaters made of sheet metal the same size as the real heaters and painted black on one Trickle To 120 V AC side. The unheated control plots had no electrical power cabling. Charger 12 V DC The PID control system was that of Kimball (2005), adapted for Baery newer equipment (Figure 4). Understory vegetation temperatures were continually measured in all plots using IR thermometers (Model FIGURE 4 Schematic diagram of components to control the SI-121, Apogee Instruments, Logan, UT). A datalogger plus multiplexor temperature rise of heated (orange) hexagonal plots above the (Model CR-1000 logger with Loggernet software and Model AM16/32 temperature of corresponding reference or control (green) plots. Additional weather instruments are also connected to the datalogger multiplexor, Campbell Scientific, Logan, UT) contained the PID logic to maintain the desired 4°C difference between the heated and control 2 plots. The logger sent signals to an interface (Model SDM-CV04, where RH is the heater capacity (W/m ), f8–14 is the fraction in the Campbell Scientific), which generated a 0–10 V signal to control the 8–14 μm waveband (assumed 0.13), ρ is the vegetation surface reflec- AC voltage supplied to the heaters. The vegetation temperatures from tance (assumed 0.02), and η is the heater array efficiency computed heated plots were adjusted for IR radiation from the IR heaters that from: was reflected from the plots and sensed by the IR thermometers η=0.10+0.25e(−0.17u) within their 8–14 μm waveband (Kimball et al., 2008). The amount of (2) reflected radiation R (W/m2) was calculated from: f where u (m/s) is wind speed (Kimball & Conley, 2009; Kimball et al., R R (PID volts 10 V)2 f f = H × ∕ × 8−14 ×ρ×η (1) 2008). To account for stochastic events (e.g., falling palm fronds) and 1936 | KIMBALL et al. random temperature spiking in individual control plots (e.g., from control panels to reduce humidity entering the casing. We also im- sunflecks), the vegetation temperatures from the control plots were plemented a regular 3-month scheduled shut-down, examination, and averaged, and then PID control signals were computed for the in- maintenance of the internal components of the control panels with dividual heated plots from the differences between the individual a certified electrician and a 6-month inspection of electrical connec- vegetation temperatures of the heated plots and the average of the tions, cabling, and grounding. Finally, we added code to the control control plots. program in the datalogger to prevent the PID signal from dropping below 0.05 V, which keeps the heaters and other equipment at a min- The control panels, designed and constructed at Watlow Electric imum of 0.5% of capacity to maintain enough residual warmth for the Manufacturing Co., contained Din-a-Mite C SCR power controllers components inside the control panels to stay dry as long as the 480 V (Model #DC2T-60C0-0000, 3-phase, 2 control leg, natural convec- power is on. tion). Each had the capacity to modulate the voltage for three heaters A weather mast was installed near the middle of the experimental (Figures 5 and 6). Thus, two Din-a-Mites were required per plot. One area to collect understory microclimatic data (Figure 2). Instruments EZ Zone PM PID Controller (Model PM6C1CC-AACAAAA) provided included a cup anemometer and wind vane (Model 03002-L, Campbell an interface between 0 and 10 V signals coming from the SDM-CV04 Scientific), pyranometer and quantum sensors (Models SP-110 and and the Din-a-Mites. The EZ Zone controller operated with 120 V SQ-110, respectively, Apogee Instruments), and an air temperature AC power, so a step-down transformer was needed to connect it to and humidity probe (Model CS215, Campbell Scientific), all connected the 480 V line power. Unfortunately, with our tropical conditions and to the same datalogger used to control the IR heater system. Weather, frequent power surges, we soon learned that, in addition to factory- canopy temperature, and heater control data were output as hourly supplied fuses, a 600 V surge protector for the main power line with averages. The wind and air sensors were deployed at 3.0 m above the three 480 V surge protectors for each plot were needed, as well as soil surface, and the radiation sensors at about 3.5 m. A thermocou- 480 V surge protectors where the line power entered each panel and ple to measure the surface temperature of one of the heaters in Plot another 120 V surge protector for the power going to the EZ Zone H4 was also connected. Rainfall data presented herein came from a controller. To ensure a safe working environment in this high voltage tipping bucket rain gauge (Model TR-525-W2; Texas Electronics, Inc.; system, we grounded each control panel, as well as every steel post of Dallas, TX USA) on a standard weather station in the open about all hexagonal plots, the primary junction boxes for each warmed plot, 200 m from the experimental site. and all dataloggers. Five soil moisture/temperature probes (Model CS655, Campbell High humidity resulted in components rusting, growing mold, and Scientific) were installed in each of the six plots and recorded hourly. creating an environment with high potential for arc flash and electrical Three probes were installed at the 0–10 cm depth: one at the center shorts. We used high heat Rustoleum paint to seal any cuts made to of each plot, a second at the edge of plot, and a third midway between the steel posts to deter rust. The control panel casing was made of center and edge. The fourth and fifth probes were installed at the painted steel. We added additional sealing to the doors of each of the 20–30 and 40–50 cm depths, respectively, at the center of the plots.

Safety switch Control panel with door lock and outside handle 480 V, 3-phase Watlow Din-A-Mite C 4-m-diameter hexagonal power input SCR Power Controllers ﬁeld plot with six Watlow #DC2T-60C0-0000 Raymax 8,100 W, 480 V, 3-phase, 2 control leg 3-phase infrared heaters 480 V surge natural convecon protector

Step-down transformer: 480 V to 120 V

120 V surge protector Wires in weatherproof conduits that provide ﬂexibility to adjust heights of the heaters ± 1.5 m from a nominal height of 3.1 m. Watlow EZ Zone PM PID Controller PM6C1CC-AACAAAA (0–10 volt DC control signal varies power 0–10 V control output to heaters from 0 to 100%) signal from datalogger FIGURE 5 Schematic diagram of a control panel KIMBALL et al. | 1937

when the project is terminated. At each of the power line junction boxes associated with the three control panels, we included 120 V power outlets to accommodate scientific equipment and small tools (Figure 2). Twelve-volt-DC sensors and dataloggers were connected to a marine battery, which in turn was connected to a 120 V AC trickle charger and a backup generator. Therefore, data collection continued during power outages and system maintenance, even when there was no power supply to the heaters. The battery also provided additional lightning protection to the logger and sensors.

2.3 | Actual and theoretical power use calculations

For six 8,100 W heaters deployed over a 4-m- diameter plot, if the system were 100% efficient, the available heating capacity would be 3,867 W/m2. By multiplying 3,867 times the PID signal (divided by FIGURE 6 Photograph of actual control panel with major 10) squared and then dividing by the measured temperature rise, the components labeled. (Photo by Aura M. Alonso-Rodríguez) actual average hourly power use per degree of temperature rise for each heated plot was obtained. The deeper probes were installed in a single 5-cm-diameter hole at a The theoretical average hourly power use per degree of tempera- 45° angle into the soil wall. ture rise for each heated plot was calculated following Kimball (2005). Power lines to the field site were conveyed in above-ground First, the IR heating requirement was calculated, which required a electrical conduits with concrete supports at about 1.5-m intervals value for canopy resistance. Measurements of stomatal conductance (Figures 2 and 3). Power lines were above-ground to minimize dis- on the understory vegetation produced an average value of about turbance to the root and soil system of the study site, to facilitate 0.038 mol m−2 s−1 (equivalent to 1,000 s/m stomatal resistance; data regular maintenance of the junction boxes, and to facilitate removal not shown), which is very low compared to most vegetation that is

4 (a) (b) 3

1 )

–1 FIGURE 7 (a) Theoretical distribution of infrared radiation at the top of vegetation –2 direction (m

surface from six heaters deployed in a Y

–3

hexagonal pattern around a 4 m-diameter in plot with no slope at a height of 1.43 m –4 above the vegetation, pointed toward 4 4 –4 (c)–3 –2 –1 0 1234(d) the center, and tilted 45° from horizontal 3 3 (following Kimball et al., 2012). (b)

Schematic diagram illustrating the average plot center 2 2 21° slope of the heated plots, the vertical posts, and the 45° tilt of infrared heaters om 1 1 with respect to the posts at the top and 0 0 bottom of the plots. (c) Like (a) but for a ance fr sloped soil surface with 1-m-tall vegetation –1 –1

and the heaters tilted 45° with respect to Dist the soil surface. The radiation is displaced –2 –2 upward (d). Like (c) but the heaters are tilted by 45° with respect to their posts as –3 –3 illustrated in (b). Some of the radiation is –4 –4 still outside the plot on the upslope side, –4 –3 –2 –1 0 1234 –3 –2 –1 01234 but much more is distributed across the plots Distance from plot center in X direction (m) 1938 | KIMBALL et al. adapted to growing in full sunlight. Leaf area index was estimated to (a) be about 0.5, and the soil was covered with dead leaves that were dry except when covered with dew or rain. Therefore, canopy resistance was estimated to also be about 1,000 s/m. However, the IR heating requirement proved quite insensitive to the estimate of canopy resistance due to the very humid conditions with low evapotranspiration. In contrast, there was more uncertainty in the aerodynamic resistance introduced by the high stall speed (0.5 m/s) of the anemometer and the calm understory conditions. Under stall conditions, wind speed was assumed to be 0.25 m/s. Next, the radiative efficiency of the heaters was calculated following Kimball (2005), and again the poor wind measurements under the very calm conditions introduced uncertainty. Finally, the theoretical IR heater requirement was divided by the radiative efficiency and the geometric efficiency for a hexagonal IR (b) heater array (0.372 from Kimball et al., 2012) to obtain the theoretical average hourly power use per degree of temperature rise.

3 | RESULTS AND DISCUSSION

3.1 | Uniformity of warming

Theoretically, a hexagonal array of IR heaters should produce uniform warming across a circular plot (Figure 7a). However, the understory vegetation in this experiment was very nonuniform, with varying height and ground coverage (Figures 3 and 8a). Consequently, the warming also appears very nonuniform (Figure 8b). Closer comparison FIGURE 8 Top. Photograph of heated plot (H4) from a ladder between Figure 8a and b, however, revealed that the hot spots cor- leaning against a tree near the plot at a height of about 7 m above responded to areas where dry leaves on the soil surface were visible. the ground. The square with dashed outline shows the approximate The areas of green vegetation, at which the IR thermometers were view of the thermal imager used to obtain the bottom thermal image from the same ladder position. For orientation, the rectangular hot pointed, were being warmed close to the target +4°C. The warming of spot at the left edge about 1/3 of the way down from the top was live foliage was therefore relatively uniform, and thus, the deployment the electrical junction box, which appears gray in the photograph. heights and angles of the six heaters were able to provide consistent The linear cooler stripe that extends from upper left downward to warming to the understory vegetation. the right is due to a vine hanging from a branch high over the plot The slope of the site also affected the IR radiation distribution. down to the soil surface. A somewhat similar cool stripe from upper Hexagonal heater arrays theoretically and actually can produce uni- right that extends downward toward the left is due to several plants in a row. The very cool leaves at the bottom left are actually above form warming on sites with zero slope (Figure 7a; Kimball et al., 2008, the height of the heaters (not considered understory) and are not 2012), and if the posts were installed at an angle from vertical equal being warmed. (photograph and image taken by Bruce Kimball) to the slope, a distribution like 7a should be possible on sloped plots. However, it is not easy to bore holes in the soil, pour concrete, and set posts at nonvertical angles, and then, the resultant structure would heated plots, soil temperatures were ~1°C warmer than the under- have a constant torque, so our posts were installed vertically. If the story vegetation temperatures at night, with less of a differential at heaters are tilted at 45° with respect to a sloped soil surface and the midday (Figure 9b). Under control conditions, there was very little spa- heater posts are vertical, theoretically the area of uniform radiation tial variability of the 0–10 cm soil temperatures across the plots from would be displaced upslope (Figure 7c). In our case, we tilted the center to edge (Figure 10b). The plot center position in the heated heaters at 45° with respect to their vertical posts (Figure 7b), rather plots, however, was slightly hotter (<1°C) than either edge or midway than the soil surface, which theoretically distributed the warming (between center and edge) positions (Figure 10b). Moreover, the IR more evenly over the plots, although some radiation still falls outside system consistently maintained the 4°C target temperature rise in sur- the plot area on the high side while the downslope edge of the plot face soils during the whole season, except when there were power receives less (Figure 7d). Nevertheless, the theoretical proportion of outages, as evidenced by the downward spikes in the curves for the total radiation falling within the plot was only reduced to 36% com- heated plots (Figure 10b). pared 39% for level plots. The temperature of the surface soils (0–10 cm) of the heated plots As expected, the IR heater array warmed the shallow soil rose to approximately 3.6°C warmer than the control plots within (Figures 9b, 10b,e and 11). At the 0–10 cm depth in the center of the 6 days of the start of warming. In contrast, the soil temperatures at KIMBALL et al. | 1939

(a) (a)

(b) (b)

(c)

(d) (e)

(e)

FIGURE 9 Infrared heater system performance during the week starting on day 36 of 2017 (130 days after the start of the warming treatment). (a) Solar radiation, rainfall (in the open), relative humidity, and wind speed. (b) Heated and control understory vegetation temperatures (± standard errors), air temperatures, and heated and FIGURE 10 Soil water contents and soil temperatures during the control soil temperatures at the 0–10 cm depth at the center of the first 6 months of the experiment in the control (Cont) and heated plots. (c) Heated minus control understory vegetation temperatures. (Heat) plots. (a) Hourly average soil water contents for 0–10 cm (d) Measured power consumption and that following the theoretical depths at the centers of the 4-m-diameter plots, at midway between equations of Kimball (2005). (e) Heated and control soil water plot centers and edges, and at the edges of the plots. The values are contents at the 0–10 cm depth in the center of the plots the means of three replicates observed at 13:00 each day. Standard errors are shown, but only for every 10 days to improve clarity. (b) both 20–30 and 40–50 cm depths were very similar to those of the Same as (a) but for soil temperatures. (c) Daily rainfall observed in the open about 200 m from the plots. (d) Soil water contents similar to (a), control plots at the start of the experiment (Figures 10e and 11), but but measured in the centers of the plots at the 0–10 cm depths, at the the temperature difference steadily increased for about a month, 20–30 cm depths, and at the 40–50 cm depths. (e) Soil temperatures leveling off at approximately +3°C warming at 20–30 and 40–50 cm similar to (b), but measured in the centers of the plots at the 0–10 cm depths, respectively, for the remaining observation period (Figures 10e depths, at the 20–30 cm depths, and at the 40–50 cm depths and 11). Averaged over the whole six months, the averaged warming was 2.9 and 2.6°C for the two depth increments, respectively (Table 2). there had been no outages. There were no sensors below 10 cm at Soil temperatures at deeper depths were less responsive to the power the edge of the plots, so we cannot be sure the warming at depth in outages, but the overall average warming may have been greater if the centers extended out to the edges. However, unlike open-top or 1940 | KIMBALL et al.

between heated and control plots. Although soil moisture was much more temporally variable than temperature (Figure 10b), there ap- peared to be little or no spatial variation in soil water content from the centers of the plots to the edges (Figure 10a). Water contents at the deeper depths were greater and fluctuated less dramatically than those at 0–10 cm (Figure 10d). From about Day 20 through Day 100, there was ample rain (Figure 10c), and consequently, the effects of heating on soil water content were not as pronounced (Figure 10a,d). However, there were four distinct drying periods during which the heated plots dried faster and more than the controls, peaking around 20, 125, 145, and 175 days from the start of the experiment (Figure 10d). Nevertheless, the average soil moisture remained adequate for the plants. While there were stronger drying events in the heated plots, over the course of 6 months of FIGURE 11 Profiles of the differences in soil temperature the warming treatment, the differences in mean soil moisture be- between heated and control plots at the 0–10, 20–30, and 40–50 cm tween the control and heated plots were not different in the surface depths that were observed at midnight 2 days before and 180 days soils (0.35 m3/m3; Table 2). The observed drying effect was overall after the start of the 4°C IR heating treatment. The sensors were at the centers of the 4-m-diameter plots. Also shown are the stronger in the deeper, more buffered soils, with the heated plots corresponding differences in vegetation canopy temperatures, which approximately 0.036/m3/m3 drier than the control plots at both have been plotted at a height of 5 cm for convenience 20–30 cm and 40–50 cm depths. It is not surprising that the warming treatment caused more soil other chambers, the warming from IR heaters generally extend outside drying. The IR warming system warms foliage and soil surface, but the defined plot area (Figures 7 and 8). For a hexagonal array, 63% of does not directly affect the absolute humidity of the air. Some obser- the IR radiation theoretically falls outside the plot area (Kimball et al., vations and global circulation models suggest that relative humidity, 2012), warming the soil under the plot edges and serving as a buffer not absolute, will remain more or less constant with global warming around the periphery. Overall, the consistent warming of surface soils (Dessler & Sherwood, 2009). On the other hand, more recent calcu- to 3.6°C and the loss of just 1°C warming with depth demonstrates lations by Sherwood and Fu (2014) suggest that, in contrast to the a strong heat holding capacity of these clayey soils, despite the high whole earth with land and ocean surfaces, global warming over the rainfall environment. Taken together, these findings suggest this IR continental land surfaces is likely to lead to overall drying, that is, a warming design can be utilized to examine the effects of warming on reduction in relative humidity and closer to warming at constant ab- soil processes as deep as 50 cm, if not more. solute humidity. Thus, the T-FACE system likely produced conditions similar to those expected with future global climate change. 3.2 | Effects on soil moisture 3.3 | Reliability and Power Issues As expected, the warming treatment resulted in a stronger dry- down of the soil of the heated plots than in the control plots during The primary obstacle to having a highly reliable warming system periods of low rain, especially in the shallow soil layer (Figures 9e was the unreliability of the main power supply to the station, which and 10a,d). However, the high rainfall environment led to rapid re- could be a common issue at numerous sites around the world. wetting with overall no difference in average soil moisture values During the first 6 months of operation from 28 September 2016

TABLE 2 Soil temperature (T) and volumetric soil moisture contents (M) for 0–10, 20–30, and 40–50 depth increments in the control and heated plots that were averaged over a year before the start of the warming treatment and for 6 months after the start of the treatment

Pretreatment (~1 year) Treatment (~6 months)

Control Heated Control Heated

Soil depth (cm) Variable Mean ± SE Range Mean ± SE Range Mean ± SE Range Mean ± SE Range

0–10 T (°C) 24.3 ± 0.08 9.15 24.3 ± 0.07 8.90 23.1 ± 0.06 8.22 26.4 ± 0.32 10.31 20–30 T (°C) 25.1 ± 0.01 3.05 25.3 ± 0.01 3.36 23.6 ± 0.02 4.22 26.5 ± 0.02 5.16 40–50 T (°C) 25.1 ± 0.01 2.56 25.2 ± 0.01 2.78 23.7 ± 0.02 3.53 26.3 ± 0.02 4.11 0–10 M (m3/m3) 0.32 ± 0.0004 0.27 0.36 ± 0.0006 0.27 0.35 ± 0.0008 0.26 0.35 ± 0.001 0.28 20–30 M (m3/m3) 0.43 ± 0.0002 0.08 0.42 ± 0.0003 0.11 0.44 ± 0.0003 0.10 0.40 ± 0.0004 0.13 40–50 M (m3/m3) 0.42 ± 0.0003 0.11 0.40 ± 0.0004 0.13 0.42 ± 0.0003 0.12 0.39 ± 0.0004 0.14 KIMBALL et al. | 1941

were working in the plots, amounting to another 1% of the total off time in the first 6 months. Fortunately, after power outages, the system rapidly re-equilibrated once power was restored. For example, there was a power outage for about 6 hr on the afternoon of DOY 37 (Figure 9). During these hours, the temperatures of the heated plots dropped close to those of the control plots (Figure 9b). After power was restored, the 4°C target was achieved within an hour. During the first 6 months, four of the 18 heaters failed and were replaced. Condensate may have formed during a power outage, result- ing in a short circuit when power was restored. Three of the heaters were in the same plot, so alternatively perhaps there was a lightning strike near this plot.

FIGURE 12 Histogram of hourly average understory vegetation temperature differences between heated and control plots between 3.4 | Performance 28 September 2016 and 28 March 2017. Individual replicates were kept separate. Hours when there were power outages were omitted. The forest understory microclimate was dark, humid, and calm The total number of observations is 9,651 (Figure 9a). Solar radiation was an order of magnitude lower than out in the open. Relative humidity was generally above 80% even at mid- to 28 March 2017 (4,350 total hours), the heaters were off 10% of day and 100% at night. Wind speeds were very low, often below the the total time due to power outages. For the safety of personnel, stall speed of the anemometer. Under these calm and humid condi- the 480 V power to individual plots was turned off when individuals tions, the IR heater system successfully maintained the +4°C target

TABLE 3 Summary of the problems encountered at this site different from those of previous infrared (IR) warming experiments and the solutions used to overcome them

Problem Solution

Power surges and outages 600 V surge protector at main power line. 480 V surge protectors in the main circuit breaker. 480 V surge protector where power line enters the control panel. 120 V surge protector where the power goes to the EZ Zone controller. Backup battery and generator power allowed data collection to occur during power outages. High humidity Liquid tight welding. Rustoleum paint to seal any cuts made to the steel posts. Control panel casing made of painted steel. Added additional sealing to the doors of each control panel. Implemented a scheduled shut-down every 3-months to examine the internal components of the control panels and provide maintenance as needed. Added code to the control program so the PID signal could not drop below 0.05 V, allowing the components inside the control panels to maintain enough residual warmth to stay dry. Steep slope with weak soils when wet Tilt of heaters 45° with respect to vertical posts (rather than soil surface). Vertical posts set in concrete. Hurricanes Civil engineer-specified design of concrete footings for the posts to withstand code design winds for the region with the heaters tilted vertical at maximum operating height (3.6 m) with no allowance for windbreak effects of the trees [withstood Hurricane Irma and Maria winds (but not falling trees)]. Movable cross-bars to lower during hurricane. Easy power off switch at the main circuit breaker. Heterogeneous understory Heater height set at 0.4 times plot diameter above three-fourth of the height of the tallest plants. The height was applied with respect to the soil surface at the bottom and top of the plots accounting for slope. Vegetation above heaters The welded lip of each IR lamp was placed around the hot front side, which was pointed downwards to minimize leaves and other debris being caught by the lip. 1942 | KIMBALL et al. increase of the understory vegetation temperatures (Figures 9b,c diameter) and a soil depth of approximately 50 cm (one-eighth plot and 12). Although there were minute-to-minute variations of the diameter). temperature rise with gusts of wind and passing clouds, the hourly Tackling the larger issue of the effects of global warming on average temperature rise was consistently within 0.1°C of the 4°C whole forest ecosystems and their climate feedbacks would ideally target (omitting hours with power outages) during the first 6 months be achieved with larger plots with adult trees. Here, we successfully of operation (Figure 12), which is excellent performance. The heaters extended both plot size and degrees of warming with heaters 4–8 were below 35% of capacity 95% of the time, so for this tropical forest times larger than previously used, which were formerly untested for understory site, we could have tripled plot areas or used equivalently this application. No scaling issues were encountered, with relatively smaller heaters. uniform warming of vegetation and soils of 4-m-diameter plots, so Surprisingly, the system maintained relatively constant heating it should be feasible to combine hexagonal arrays into honeycombs under rainy conditions. For example, 11 mm of rain was received on as suggested by Kimball et al. (2012) and extrapolate to 30-m-tall DOY 38, enough to significantly increase soil moisture at the 10 cm trees and the 100-m scale plots needed for forest and orchard depth (Figure 9e), yet the temperature rise of the heated plots dropped experiments. only one degree below the 4°C target (Figure 9b,c). The actual measured power consumption per degree of tempera- ACKNOWLEDGMENTS ture rise was generally only 100 W m−2 °C−1 (Figure 9d), which is somewhat low, but consistent with the calm, humid conditions. The We gratefully acknowledge the technical assistance of Carlos Estrada, theoretical curve is generally lower than the measured values but Carlos Torrens, Amelia Dávila, Adolfo Menéndez, and Yolanda near the lower error bar values, which again gives credence to the Padilla. Skip van Bloem, Richard Norby, Roy Rich, Ariel E. Lugo, and theoretical equations that can be used to aid in the design of future Keith Lewin, provided invaluable technical advice. We are grateful experiments. to comments from Tim Wertin and two anonymous reviewers, which significantly improved the paper. This research was supported by USDA Forest Service awards to BAK (14-JV-11120101-006), SCR 4 | CONCLUSIONS AND IMPLICATIONS (13-IA-11120101-008), MAC (13-JV-11120101-033) and TEW (11-DG-11120101-012) as well as US Department of Energy Office For millennia, tropical forests have persisted under a relatively sta- of Science grants to SCR, TEW and MAC (DE-SC0012000 and DE- ble thermal environment; yet, in the next 80 years, climate change is SC-0011806). GG was supported by National Science Foundation expected to increase global temperatures by up to 4°C (IPCC, 2014). to the Luquillo Critical Zone Observatory (EAR-1331841) and the Because tropical species are adapted to very narrow thermal niches, Luquillo Long Term Ecological Research Program (DEB 1239764). their ability to tolerate and acclimate to increased temperatures may The Puerto Rico Conservation Foundation, USDA Forest Service be much more limited than in higher-latitude ecosystems (Janzen, International Institute of Tropical Forestry, and The University of 1967). If true, relatively small increases in temperature could have Puerto Rico provided additional support. Any trade, product, or firm very large consequences for the substantial amounts of carbon cycled name is used for descriptive purposes only and does not imply en- by tropical forests. Until now, logistical challenges such as high rainfall dorsement by the U.S. Government. and humidity and inconsistent power have meant that the field warming experiments, which have been so influential in our understand- CONFLICT OF INTEREST ing of ecosystem responses to warming in other biomes, have been absent in tropical forests. Here, we describe solutions developed in None declared. response to these unique challenges, providing a significant step for- ward in our ability to experimentally warm a wider range of ecosystem AUTHOR CONTRIBUTIONS types. As a whole, the IR Heater system maintained the target 4°C rise TW, MC, and SR involved in conceptualizing and planning experiment; in temperature of the heated plots above that of the controls when BK, TW, and GG involved in design of warming system and power in- power was available (Figure 12), and uniformity of the treatment ef- frastructure; TW, BK, GG, and AA involved in construction and instal- fect was satisfactory (Figure 8). Furthermore, the system achieved lation of heater system and power upgrades; TW and AA performed significant soil warming of 2.6°C on average to a depth of 50 cm maintenance of experiment; SR, MC, TW, and AA performed installa- with minimal soil drying. To achieve this success, several obstacles tion of soil and plant sensors and making measurements; all involved were addressed (Table 3). Thus, based on our experience reported in writing and editing the manuscript. herein and that of many prior experiments listed in the Introduction, our system can be used to study tropical and nontropical forest un- ORCID derstory plants and soils, as well as agricultural crops and range- land, up to a vegetation height of at least 1.3 m (one-third the plot Bruce A. Kimball http://orcid.org/0000-0003-3009-061X KIMBALL et al. | 1943

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